Host-pathogen interactions under pressure: A review and meta-analysis of stress-mediated effects on disease dynamics.
environmental stress
epidemiological models
fecundity
infectivity
pollution
resource limitation
survival
Journal
Ecology letters
ISSN: 1461-0248
Titre abrégé: Ecol Lett
Pays: England
ID NLM: 101121949
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
07
09
2023
received:
27
03
2023
accepted:
12
09
2023
medline:
2
11
2023
pubmed:
7
10
2023
entrez:
7
10
2023
Statut:
ppublish
Résumé
Human activities have increased the intensity and frequency of natural stressors and created novel stressors, altering host-pathogen interactions and changing the risk of emerging infectious diseases. Despite the ubiquity of such anthropogenic impacts, predicting the directionality of outcomes has proven challenging. Here, we conduct a review and meta-analysis to determine the primary mechanisms through which stressors affect host-pathogen interactions and to evaluate the impacts stress has on host fitness (survival and fecundity) and pathogen infectivity (prevalence and intensity). We assessed 891 effect sizes from 71 host species (representing seven taxonomic groups) and 78 parasite taxa from 98 studies. We found that infected and uninfected hosts had similar sensitivity to stressors and that responses varied according to stressor type. Specifically, limited resources compromised host fecundity and decreased pathogen intensity, while abiotic environmental stressors (e.g., temperature and salinity) decreased host survivorship and increased pathogen intensity, and pollution increased mortality but decreased pathogen prevalence. We then used our meta-analysis results to develop susceptible-infected theoretical models to illustrate scenarios where infection rates are expected to increase or decrease in response to resource limitations or environmental stress gradients. Our results carry implications for conservation and disease emergence and reveal areas for future work.
Types de publication
Meta-Analysis
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2003-2020Subventions
Organisme : Emory University
Organisme : Fulbright
Organisme : Halle Institute for Global Research, Emory University
Organisme : National Institute of Allergy and Infectious Diseases
ID : 1R01 AI150774
Organisme : NSF IOS
ID : 1755002
Organisme : Vetenskapsrådet
ID : 2019-06444
Informations de copyright
© 2023 John Wiley & Sons Ltd.
Références
Alford, R.A., Bradfield, K.S. & Richards, S.J. (2007) Global warming and amphibian losses. Nature, 447, E3-E4.
Allen, T., Murray, K.A., Zambrana-Torrelio, C., Morse, S.S., Rondinini, C., Di Marco, M. et al. (2017) Global hotspots and correlates of emerging zoonotic diseases. Nature Communications, 8, 1124.
Alonso-Alvarez, C. & Tella, J.L. (2001) Effects of experimental food restriction and body-mass changes on the avian T-cell-mediated immune response. Canadian Journal of Zoology, 79, 101-105.
Anderson, A.R.M., May, R.M., Joysey, K., Mollison, D., Conway, G.R., Cartwell, R. et al. (1986) The invasion, persistence and spread of infectious diseases within animal and plant communities. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 314(1167), 533-570.
Anderson, R.M. & May, R.M. (1991) Infectious diseases of humans: dynamics and control. New York: Oxford University Press.
Arnold, T.W. (2010) Uninformative parameters and model selection using akaike's information criterion. Journal of Wildlife Management, 74, 1175-1178.
Ayres, J.S. & Schneider, D.S. (2009) The role of anorexia in resistance and tolerance to infections in Drosophila. PLoS Biology, 7, e1000150.
Barnosky, A.D., Hadly, E.A., Bascompte, J., Berlow, E.L., Brown, J.H., Fortelius, M. et al. (2012) Approaching a state shift in Earth's biosphere. Nature, 486, 52-58.
Barron, D.G., Gervasi, S.S., Pruitt, J.N. & Martin, L.B. (2015) Behavioral competence: how host behaviors can interact to influence parasite transmission risk. Current Opinion in Behavioral Sciences, 6, 35-40.
Bartón, K. (2023) MuMIn: Multi-Model Inference (R package version 1.47.5). Available from: https://cran.r-project.org/package=MuMIn [Accessed 7th September 2023].
Becker, D.J., Eby, P., Madden, W., Peel, A.J. & Plowright, R.K. (2023) Ecological conditions predict the intensity of Hendra virus excretion over space and time from bat reservoir hosts. Ecology Letters, 26, 23-36.
Becker, D.J. & Hall, R.J. (2014) Too much of a good thing: resource provisioning alters infectious disease dynamics in wildlife. Biology Letters, 10, 20140309.
Becker, D.J., Streicker, D.G. & Altizer, S. (2015) Linking anthropogenic resources to wildlife-pathogen dynamics: a review and meta-analysis. Ecology Letters, 18, 483-495.
Beldomenico, P.M. & Begon, M. (2016) Stress-host-parasite interactions: a vicious triangle? Revista FAVE. Sección Ciencias veterinarias, 14, 6-19.
Boots, M. (2008) Fight or learn to live with the consequences? Trends in Ecology & Evolution, 23, 248-250.
Bruno, J.F., Selig, E.R., Casey, K.S., Page, C.A., Willis, B.L., Harvell, C.D. et al. (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biology, 5, e124.
Buck, J.C., Weinstein, S.B. & Young, H.S. (2018) Ecological and evolutionary consequences of parasite avoidance. Trends in Ecology & Evolution, 33, 619-632.
Byers, J.E. (2021) Marine parasites and disease in the era of global climate change. Annual Review of Marine Science, 13, 397-420.
Caren, L.D. (1981) Environmental pollutants: effects on the immune system and resistance to infectious disease. Bioscience, 31, 582-586.
Casadevall, A. & Pirofski, L.-A. (2002) What is a pathogen? Annals of Medicine, 34, 2-4.
Charlier, J., Barkema, H.W., Becher, P., De Benedictis, P., Hansson, I., Hennig-Pauka, I. et al. (2022) Disease control tools to secure animal and public health in a densely populated world. Lancet Planetary Health, 6, e812-e824.
Cheng, T.L., Reichard, J.D., Coleman, J.T.H., Weller, T.J., Thogmartin, W.E., Reichert, B.E. et al. (2021) The scope and severity of white-nose syndrome on hibernating bats in North America. Conservation Biology, 35, 1-12.
Christe, P., Richner, H. & Oppliger, A. (1996) Begging, food provisioning, and nestling competition in great tit broods infested with ectoparasites. Behavioral Ecology, 7, 127-131.
Civitello, D.J., Allman, B.E., Morozumi, C. & Rohr, J.R. (2018) Assessing the direct and indirect effects of food provisioning and nutrient enrichment on wildlife infectious disease dynamics. Philosophical Transactions of the Royal Society B: Biological Sciences, 373, 20170101.
Civitello, D.J., Angelo, T., Nguyen, K.H., Hartman, R.B., Starkloff, N.C., Mahalila, M.P. et al. (2022) Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts. Proceedings of the National Academy of Sciences of the United States of America, 119, e2116512119.
Civitello, D.J., Penczykowski, R.M., Smith, A.N., Shocket, M.S., Duffy, M.A. & Hall, S.R. (2015) Resources, key traits and the size of fungal epidemics in Daphnia populations. The Journal of Animal Ecology, 84, 1010-1017.
Cohen, J.M., Civitello, D.J., Venesky, M.D., McMahon, T.A. & Rohr, J.R. (2019) An interaction between climate change and infectious disease drove widespread amphibian declines. Global Change Biology, 25, 927-937.
Cohen, J.M., McMahon, T.A., Ramsay, C., Roznik, E.A., Sauer, E.L., Bessler, S. et al. (2019) Impacts of thermal mismatches on chytrid fungus Batrachochytrium dendrobatidis prevalence are moderated by life stage, body size, elevation and latitude. Ecology Letters, 22, 817-825.
Cohen, J.M., Sauer, E.L., Santiago, O., Spencer, S. & Rohr, J.R. (2020) Divergent impacts of warming weather on wildlife disease risk across climates. Science, 370, eabb1702.
Crain, C.M., Kroeker, K. & Halpern, B.S. (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecology Letters, 11, 1304-1315.
Cressler, C.E., Nelson, W.A., Day, T. & McCauley, E. (2014) Disentangling the interaction among host resources, the immune system and pathogens. Ecology Letters, 17, 284-293.
Cumnock, K., Gupta, A.S., Lissner, M., Chevee, V., Davis, N.M. & Schneider, D.S. (2018) Host energy source is important for disease tolerance to malaria. Current Biology, 28, 1635-1642.e3.
Dallas, T. & Drake, J.M. (2014) Nitrate enrichment alters a Daphnia - microparasite interaction through multiple pathways. Ecology and Evolution, 4, 243-250.
de Castro, F. & Bolker, B.M. (2005) Parasite establishment and host extinction in model communities. Oikos, 111, 501-513.
Del Giudice, M., Buck, C.L., Chaby, L.E., Gormally, B.M., Taff, C.C., Thawley, C.J. et al. (2018) What is stress? A systems perspective. Integrative and Comparative Biology, 58, 1019-1032.
Dirzo, R., Young, H.S., Galetti, M., Ceballos, G., Isaac, N.J.B. & Collen, B. (2014) Defaunation in the Anthropocene. Science, 345, 401-406.
Douglas, B. & Maechler, M. (2021) Matrix: sparse and dense matrix classes and methods. R package Matrix version 1.4-0. R Packag. version 0.999375-43. Available from: https://cran.r-project.org/package=Matrix [Accessed 17th February 2022].
Eberhardt, A.T., Costa, S.A., Marini, M.R., Racca, A., Baldi, C.J., Robles, M.R. et al. (2013) Parasitism and physiological trade-offs in stressed capybaras. PLoS One, 8, e70382.
Eby, P., Peel, A.J., Hoegh, A., Madden, W., Giles, J.R., Hudson, P.J. et al. (2023) Pathogen spillover driven by rapid changes in bat ecology. Nature, 613, 340-344.
Epstein, J.H., McKee, J., Shaw, P., Hicks, V., Micalizzi, G., Daszak, P. et al. (2006) The Australian white ibis (Threskiornis molucca) as a reservoir of zoonotic and livestock pathogens. EcoHealth, 3, 290-298.
Exton, M.S. (1997) Infection-induced anorexia: active host defence strategy. Appetite, 29, 369-383.
Eze, J.I., Okeke, M.C., Ngene, A.A., Omeje, J.N. & Abonyi, F.O. (2013) Effects of dietary selenium supplementation on parasitemia, anemia and serum proteins of Trypanosoma brucei brucei infected rats. Experimental Parasitology, 135, 331-336.
Faust, C.L., Dobson, A.P., Gottdenker, N., Bloomfield, L.S.P., McCallum, H.I., Gillespie, T.R. et al. (2017) Null expectations for disease dynamics in shrinking habitat: dilution or amplification? Philosophical Transactions of the Royal Society B, 372, 20160173.
Faust, C.L., McCallum, H.I., Bloomfield, L.S.P., Gottdenker, N.L., Gillespie, T.R., Torney, C.J. et al. (2018) Pathogen spillover during land conversion. Ecology Letters, 21, 471-483.
Garner, T.W.J., Walker, S., Bosch, J., Leech, S., Rowcliffe, J.M., Cunningham, A.A. et al. (2009) Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos, 118, 783-791.
Gervasi, S.S., Civitello, D.J., Kilvitis, H.J. & Martin, L.B. (2015) The context of host competence: a role for plasticity in host-parasite dynamics. Trends in Parasitology, 31, 419-425.
Ghandour, A.M. & Webbe, G. (1975) The effect of sublethal concentrations of the molluscicide niclosamide on the infectivity of Schistosoma mansoni cercariae. Journal of Helminthology, 49, 245-250.
Gheorgiu, C., Cable, J., Marcogliese, D.J. & Scott, M.E. (2007) Effects of waterborne zinc on reproduction, survival and morphometrics of Gyrodactylus turnbulli (Monogenea) on guppies (Poecilia reticulata). International Journal for Parasitology, 37, 375-381.
Gheorgiu, C., Marcogliese, D.J. & Scott, M. (2006) Concentration-dependent effects of waterborne zinc on population dynamics of Gyrodactylus turnbulli (Monogenea) on isolated guppies (Poecilia reticulata). Parasitology, 132, 225-232.
Gibb, R., Redding, D.W., Chin, K.Q., Donnelly, C.A., Blackburn, T.M., Newbold, T. et al. (2020) Zoonotic host diversity increases in human-dominated ecosystems. Nature, 584, 398-402.
Gustafsson, L., Nordling, D., Andersson, M.S., Sheldon, B.C. & Qvarnstrom, A. (1994) Infectious diseases, reproductive effort and the cost of reproduction in birds. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 346, 323-331.
Hall, S.R., Knight, C.J., Becker, C.R., Duffy, M.A., Tessier, A.J. & Cáceres, C.E. (2009) Quality matters: resource quality for hosts and the timing of epidemics. Ecology Letters, 12, 118-128.
Hall, S.R., Simonis, J.L., Nisbet, R.M., Tessier, A.J. & Cáceres, C.E. (2009) Resource ecology of virulence in a planktonic host-parasite system: an explanation using dynamic energy budgets. The American Naturalist, 174, 149-162.
Han, B.A., Kramer, A.M. & Drake, J.M. (2016) Global patterns of zoonotic disease in mammals. Trends in Parasitology, 32, 565-577.
Harvell, C.D., Mitchell, C.E., Ward, J.R., Altizer, S., Dobson, A.P., Ostfeld, R.S. et al. (2002) Climate warming and disease risks for terrestrial and marine biota. Science, 296, 2158-2162.
Hasselblad, V. & Hedges, L.V. (1995) Meta-analysis of screening and diagnostic tests. Psychological Bulletin, 117, 167-178.
Haydon, D.T., Cleaveland, S., Taylor, L.H. & Laurenson, M.K. (2002) Identifying reservoirs of infection: a conceptual and practical challenge. Emerging Infectious Diseases, 8, 1468-1473.
Hedges, L.V. (1981) Distribution theory for Glass's estimator of effect size and related estimators. Journal of Educational Statistics, 6, 107-128.
Hedges, L.V., Tipton, E. & Johnson, M.C. (2010) Robust variance estimation in meta-regression with dependent effect size estimates. Research Synthesis Methods, 1, 39-65.
Higgins, J.P.T. & Thompson, S.G. (2002) Quantifying heterogeneity in a meta-analysis. Statistics in Medicine, 21, 1539-1558.
Hite, J.L., Pfenning, A.C. & Cressler, C.E. (2020) Starving the enemy? Feeding behavior shapes host-parasite interactions. Trends in Ecology & Evolution, 35, 68-80.
Hopkins, S.R., Fleming-Davies, A.E., Belden, L.K. & Wojdak, J.M. (2020) Systematic review of modeling assumptions and empirical evidence: does parasite transmission increase nonlinearly with host density? Methods in Ecology and Evolution, 2020, 1-11.
Hozo, S.P., Djulbegovic, B. & Hozo, I. (2005) Estimating the mean and variance from the median, range, and the size of a sample. BMC Medical Research Methodology, 5, 13.
Johnson, M.B., Lafferty, K.D., van Oosterhout, C. & Cable, J. (2011) Parasite transmission in social interacting hosts: monogenean epidemics in guppies. PLoS One, 6, e22634.
Johnson, P.T.J., Rohr, J.R., Hoverman, J.T., Kellermanns, E., Bowerman, J. & Lunde, K.B. (2012) Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecology Letters, 15, 235-242.
Johnson, P.T.J., Townsend, A.R., Cleveland, C.C., Glibert, P.M., Howarth, R.W., McKenzie, V.J. et al. (2010) Linking environmental nutrient enrichment and disease emergence in humans and wildlife. Ecological Applications, 20, 16-29.
Jones, K.E., Patel, N.G., Levy, M.A., Storeygard, A., Balk, D., Gittleman, J.L. et al. (2008) Global trends in emerging infectious diseases. Nature, 451, 990-993.
Kiesecker, J.M. (2002) Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proceedings of the National Academy of Sciences of the United States of America, 99, 9900-9904.
King, C.L. & Higashi, G.I. (1992) Schistosoma mansoni: silver ion (Ag+) stimulates and reversibly inhibits lipid-induced cercarial penetration. Experimental Parasitology, 75, 31-39.
Kluger, M.J., Kozak, W., Conn, C.A., Leon, L.R. & Soszynski, D. (1996) The adaptive value of fever. Infectious Disease Clinics of North America, 10, 1-20.
Knutie, S.A., Wilkinson, C.L., Wu, Q.C., Ortega, C.N. & Rohr, J.R. (2017) Host resistance and tolerance of parasitic gut worms depend on resource availability. Oecologia, 183, 1031-1040.
Kyriazakia, I., Tolkamp, B.J. & Hutchings, M.R. (1998) Towards a functional explanation for the occurrence of anorexia during parasitic infections. Animal Behaviour, 56, 265-274.
Lafferty, K.D. (2004) Fishing for lobsters indirectly increases epidemics in sea urchins. Ecological Applications, 14, 1566-1573.
Lafferty, K.D. (2017) Marine infectious disease ecology. Annual Review of Ecology, Evolution, and Systematics, 48, 473-496.
Lafferty, K.D. & Holt, R.D. (2003) How should environmental stress affect the population dynamics of disease? Ecology Letters, 6, 654-664.
Lajeunesse, M.J. (2013) Recovering missing or partial data from studies: a survey of conversions and imputations for meta-analysis. In: Koricheva, J., Gurevitch, J. & Mengersen, K. (Eds.) Handbook of meta-analysis in ecology and evolution. Princeton, New Jersey: Princeton University Press, pp. 195-206.
Langwig, K.E., Frick, W.F., Bried, J.T., Hicks, A.C., Kunz, T.H. & Marm Kilpatrick, A. (2012) Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecology Letters, 15, 1050-1057.
Langwig, K.E., Frick, W.F., Hoyt, J.R., Parise, K.L., Drees, K.P., Kunz, T.H. et al. (2016) Drivers of variation in species impacts for a multi-host fungal disease of bats. Philosophical Transactions of the Royal Society B: Biological Sciences, 371, 20150456.
Lloyd-Smith, J.O., Schreiber, S.J., Kopp, P.E. & Getz, W.M. (2005) Superspreading and the effect of individual variation on disease emergence. Nature, 438, 355-359.
Lochmiller, R.L. & Deerenberg, C. (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos, 88, 87-98.
Lötters, S., Kielgast, J., Bielby, J., Schmidtlein, S., Bosch, J., Veith, M. et al. (2009) The link between rapid enigmatic amphibian decline and the globally emerging chytrid fungus. EcoHealth, 6, 358-372.
Luis, A.D., Hayman, D.T.S., O'Shea, T.J., Cryan, P.M., Gilbert, A.T., Pulliam, J.R.C. et al. (2013) A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proceedings of the Royal Society B: Biological Sciences, 280, 20122753.
Maizels, R.M. & Yazdanbakhsh, M. (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Reviews. Immunology, 3, 733-744.
Marcogliese, D.J. (2008) The impact of climate change on the parasites and infectious diseases of aquatic animals. Revue Scientifique et Technique, 27, 467-484.
Marcogliese, D.J. & Pietrock, M. (2011) Combined effects of parasites and contaminants on animal health: parasites do matter. Trends in Parasitology, 27, 123-130.
Maynard, J., van Hooidonk, R., Eakin, C.M., Puotinen, M., Garren, M., Williams, G. et al. (2015) Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence. Nature Climate Change, 5, 688-694.
McCallum, H., Barlow, N. & Hone, J. (2001) How should pathogen transmission be modeled? Trends in Ecology & Evolution, 16, 295-300.
McCallum, H.I., Kuris, A., Harvell, C.D., Lafferty, K., Smith, G.W. & Porter, J. (2004) Does terrestrial epidemiology apply to marine systems? Trends in Ecology & Evolution, 19, 585-591.
McKenzie, V.J. & Townsend, A.R. (2007) Parasitic and infectious disease responses to changing global nutrient cycles. EcoHealth, 4, 384-396.
McNew, S.M., Knutie, S.A., Goodman, G.B., Theodosopoulos, A., Saulsberry, A., Yépez, R.J. et al. (2019) Annual environmental variation influences host tolerance to parasites. Proceedings of the Royal Society B: Biological Sciences, 286, 20190049.
Measures, L.N. (1996) Effect of temperature and salinity on development and survival of eggs and free-living larvae of sealworm (Pseudoterranova decipiens). Canadian Journal of Fisheries and Aquatic Sciences, 53, 2804-2807.
Medzhitov, R., Schneider, D.S. & Soares, M.P. (2012) Disease tolerance as a defense strategy. Science, 335, 936-941.
Morley, N.J., Crane, M. & Lewis, J.W. (2002) Toxic effects of cadmium and zinc on the transmission of Echinoparyphium recurvatum cercariae. Journal of Helminthology, 76, 157-163.
Murray, M.J. & Murray, A.B. (1979) Anorexia of infection as a mechanism of host defense. The American Journal of Clinical Nutrition, 32, 593-596.
Nakagawa, S., Lagisz, M., Jennions, M.D., Koricheva, J., Noble, D.W.A., Parker, T.H. et al. (2022) Methods for testing publication bias in ecological and evolutionary meta-analyses. Methods in Ecology and Evolution, 13, 4-21.
Nakagawa, S., Lagisz, M., O'Dea, R.E., Rutkowska, J., Yang, Y., Noble, D.W.A. et al. (2021) The orchard plot: cultivating a forest plot for use in ecology, evolution, and beyond. Research Synthesis Methods, 12, 4-12.
Nakagawa, S. & Santos, E.S.A. (2012) Methodological issues and advances in biological meta-analysis. Evolutionary Ecology, 26, 1253-1274.
Owen, J.C., Landwerlen, H.R., Dupuis, A.P., Belsare, A.V., Sharma, D.B., Wang, S. et al. (2021) Reservoir hosts experiencing food stress alter transmission dynamics for a zoonotic pathogen. Proceedings of the Royal Society B: Biological Sciences, 288, 20210881.
Pap, P.L., Vágási, C.I., Vincze, O., Osváth, G., Veres-Szászka, J. & Czirják, G.Á. (2015) Physiological pace of life: the link between constitutive immunity, developmental period, and metabolic rate in European birds. Oecologia, 177, 147-158.
Pechenik, J.A. & Fried, B. (1995) Effect of temperature on survival and infectivity of Echinostoma trivolvis cercariae: a test of the energy limitation hypothesis. Parasitology, 111, 373-378.
Pietrock, M. & Marcogliese, D.J. (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology, 19, 293-299.
Plowright, R.K., Eby, P., Hudson, P.J., Smith, I.L., Westcott, D., Bryden, W.L. et al. (2015) Ecological dynamics of emerging bat virus spillover. Proceedings of the Royal Society B: Biological Sciences, 282, 20142124.
Plowright, R.K., Parrish, C.R., McCallum, H., Hudson, P.J., Ko, A.I., Graham, A.L. et al. (2017) Pathways to zoonotic spillover. Nature Reviews. Microbiology, 15, 502-510.
Pölkki, M., Kangassalo, K. & Rantala, M.J. (2012) Transgenerational effects of heavy metal pollution on immune defense of the Blow Fly Protophormia terraenovae. PLoS One, 7, e38832.
Prentice, J.C., Fox, N.J., Hutchings, M.R., White, P.C.L., Davidson, R.S. & Marion, G. (2019) When to kill a cull: factors affecting the success of culling wildlife for disease control. Journal of the Royal Society Interface, 16, 20180901.
Previtali, M.A., Ostfeld, R.S., Keesing, F., Jolles, A.E., Hanselmann, R. & Martin, L.B. (2012) Relationship between pace of life and immune responses in wild rodents. Oikos, 121, 1483-1492.
Pulkkinen, K. & Ebert, D. (2004) Host starvation decreases parasite load and mean host size in experimental populations. Ecology, 85, 823-833.
Pustejovsky, J.E. (2020) clubSandwich: Cluster-Robust (Sandwich) Variance Estimators with Small-Sample Corrections (0.4.2) [R package]. Available from: https://github.com/jepusto/clubSandwich [Accessed 17th February 2022].
R Core Team. (2013) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from http://www.R-project.org
Råberg, L., Graham, A.L. & Read, A.F. (2009) Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 37-49.
Råberg, L., Sim, D. & Read, A.F. (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science, 318, 812-814.
Reading, C.J. (2007) Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia, 151, 125-131.
Riggs, M.R., Lemly, A.D. & Esch, G.W. (1987) The growth, biomass, and fecundity of Bothriocephalus acheilognathi in a North Carolina cooling reservoir. The Journal of Parasitology, 73, 893-900.
Rimbach, R., Bisanzio, D., Galvis, N., Link, A., Di Fiore, A. & Gillespie, T.R. (2015) Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics. Philosophical Transactions of the Royal Society B, 370, 20140110.
Rodrigues, M.A., Merckelbach, A., Durmaz, E., Kerdaffrec, E. & Flatt, T. (2021) Transcriptomic evidence for a trade-off between germline proliferation and immunity in Drosophila. Evolution Letters, 5, 644-656.
Rohr, J.R., Barrett, C.B., Civitello, D.J., Craft, M.E., Delius, B., DeLeo, G.A. et al. (2019) Emerging human infectious diseases and the links to global food production. Nature Sustainability, 26(2), 445-456.
Rohr, J.R. & Raffel, T.R. (2010) Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proceedings of the National Academy of Sciences of the United States of America, 107, 8269-8274.
Rohr, J.R., Schotthoefer, A.M., Raffel, T.R., Carrick, H.J., Halstead, N., Hoverman, J.T. et al. (2008) Agrochemicals increase trematode infections in a declining amphibian species. Nature, 455, 1235-1239.
Rollins-Smith, L.A., Ramsey, J.P., Pask, J.D., Reinert, L.K. & Woodhams, D.C. (2011) Amphibian immune defenses against chytridiomycosis: impacts of changing environments. Integrative and Comparative Biology, 51, 552-562.
Rosenberg, M.S., Rothstein, H.R. & Gurevitch, J. (2013) Effect sizes: conventional choices and calculations. In: Koricheva, J., Gurevitch, J. & Mengersen, K. (Eds.) Handbook of meta-analysis in ecology and evolution. Princeton, New Jersey: Princeton University Press, pp. 61-71.
Rushmore, J., Bisanzio, D. & Gillespie, T.R. (2017) Making new connections: insights from primate-parasite networks. Trends in Parasitology, 33, 547-560.
Ryder, J.J., Miller, M.R., White, A., Knell, R.J. & Boots, M. (2007) Host-parasite population dynamics under combined frequency- and density-dependent transmission. Oikos, 116, 2017-2026.
Sánchez, C.A., Altizer, S. & Hall, R.J. (2020) Landscape-level toxicant exposure mediates infection impacts on wildlife populations. Biology Letters, 16, 20200559.
Satterfield, D.A., Marra, P.P., Sillett, T.S. & Altizer, S. (2018) Responses of migratory species and their pathogens to supplemental feeding. Philosophical Transactions of the Royal Society B: Biological Sciences, 373, 20170094.
Scheele, B.C., Pasmans, F., Skerratt, L.F., Berger, L., Martel, A., Beukema, W. et al. (2019) Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science, 363, 1459-1463.
Schmid-Hempel, P. (2008) Parasite immune evasion: a momentous molecular war. Trends in Ecology & Evolution, 23, 318-326.
Schneider, D.S. & Ayres, J.S. (2008) Two ways to survive infection: what resistance and tolerance can teah us about treating infectious diseases. Nature Reviews. Immunology, 8, 889-895.
Schwenke, R.A., Lazzaro, B.P. & Wolfner, M.F. (2016) Reproduction-immunity trade-offs in insects. Annual Review of Entomology, 61, 239-256.
Sheldon, B.C. & Verhulst, S. (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution, 11, 317-321.
Soetaert, K., Petzoldt, T. & Setzer, R.W. (2010) Solving Differential Equations in R: Package deSolve. Journal of Statistical Software, 33, 1-25.
Stanley, T.D. & Doucouliagos, H. (2014) Meta-regression approximations to reduce publication selection bias. Research Synthesis Methods, 5, 60-78.
Strauss, A.T., Civitello, D.J., Cáceres, C.E. & Hall, S.R. (2015) Success, failure and ambiguity of the dilution effect among competitors. Ecology Letters, 18, 916-926.
Strauss, A.T., Shocket, M.S., Civitello, D.J., Hite, J.L., Penczykowski, R.M., Duffy, M.A. et al. (2016) Habitat, predators, and hosts regulate disease in Daphnia through direct and indirect pathways. Ecological Monographs, 86, 393-411.
Streicker, D.G., Fenton, A. & Pedersen, A.B. (2013) Differential sources of host species heterogeneity influence the transmission and control of multihost parasites. Ecology Letters, 16, 975-984.
Studer, A., Thieltges, D. & Poulin, R. (2010) Parasites and global warming: net effects of temperature on an intertidal host-parasite system. Marine Ecology Progress Series, 415, 11-22.
Svensson, E.I. & Råberg, L. (2010) Resistance and tolerance in animal enemy-victim coevolution. Trends in Ecology & Evolution, 25, 267-274.
Viechtbauer, W. (2010) Conducting meta-analyses in R with the metafor package. Journal of Statistical Software, 36, 1-48.
Wan, X., Wang, W., Liu, J. & Tong, T. (2014) Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Medical Research Methodology, 14, 135.
Wang, A., Huen, S.C., Luan, H.H., Yu, S., Zhang, C., Gallezot, J.-D. et al. (2016) Opposing effects of fasting metabolism on tissue tolerance in bacterial and viral inflammation. Cell, 166, 1512-1525.e12.
Ward, J., Kim, K. & Harvell, C. (2007) Temperature affects coral disease resistance and pathogen growth. Marine Ecology Progress Series, 329, 115-121.
Wiethoelter, A.K., Beltrán-Alcrudo, D., Kock, R. & Mor, S.M. (2015) Global trends in infectious diseases at the wildlife - livestock interface. Proceedings of the National Academy of Sciences of the United States of America, 112, 9662-9667.
Woolhouse, M.E.J., Taylor, L.H. & Haydon, D.T. (2001) Population biology of multihost pathogens. Science, 292, 1109-1112.
Yates, F. (1934) Contingency tables involving small numbers and the chi-squared test. Supplement to the Journal of the Royal Statistical Society, 1, 235.